The Phylogeography of Indoplanorbis Exustus (Gastropoda: Planorbidae) in Asia Parasites & Vectors 2010, 3:57
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Liu et al. Parasites & Vectors 2010, 3:57 http://www.parasitesandvectors.com/content/3/1/57 RESEARCH Open Access TheResearch phylogeography of Indoplanorbis exustus (Gastropoda: Planorbidae) in Asia Liang Liu1, Mohammed MH Mondal2, Mohamed A Idris3, Hakim S Lokman4, PRV Jayanthe Rajapakse5, Fadjar Satrija6, Jose L Diaz7, E Suchart Upatham8,9 and Stephen W Attwood*1,10 Abstract Background: The freshwater snail Indoplanorbis exustus is found across India, Southeast Asia, central Asia (Afghanistan), Arabia and Africa. Indoplanorbis is of economic importance in that it is responsible for the transmission of several species of the genus Schistosoma which infect cattle and cause reduced livestock productivity. The snail is also of medical importance as a source of cercarial dermatitis among rural workers, particularly in India. In spite of its long history and wide geographical range, it is thought that Indoplanorbis includes only a single species. The aims of the present study were to date the radiation of Indoplanorbis across Asia so that the factors involved in its dispersal in the region could be tested, to reveal potential historical biogeographical events shaping the phylogeny of the snail, and to look for signs that I. exustus might be polyphyletic. Results: The results indicated a radiation beginning in the late Miocene with a divergence of an ancestral bulinine lineage into Assam and peninsular India clades. A Southeast Asian clade diverged from the peninsular India clade late- Pliocene; this clade then radiated at a much more rapid pace to colonize all of the sampled range of Indoplanorbis in the mid-Pleistocene. Conclusions: The phylogenetic depth of divergences between the Indian clades and Southeast Asian clades, together with habitat and parasitological differences suggest that I. exustus may comprise more than one species. The timescale estimated for the radiation suggests that the dispersal to Arabia and to Southeast Asia was facilitated by palaeogeographical events and climate change, and did not require human involvement. Further samples from Afghanistan, Africa and western India are required to refine the phylogeographical hypothesis and to include the African Recent dispersal. Background by I. exustus. Although other snails have been implicated The medical importance of Indoplanorbis in transmission of these three Schistosoma spp. (e.g., Lym- The freshwater snail Indoplanorbis exustus (Deshayes, naea luteola, S. indicum and S. nasale and Lymnaea 1834) (Planorbidae: Bulininae) is the sole member of its acuminata, S. nasale and S. spindale), I. exustus is the genus and is widely distributed across the tropics as an most important host for S. nasale and S. spindale, as well important intermediate host for several trematode para- as for S. indicum in certain regions. Indeed I. exustus may sites (Trematoda: Digenea). I. exustus is best known as be the sole natural intermediate host for these three the intermediate host responsible for the transmision of Schistosoma species on the Indian sub-continent[3]. The Schistosoma nasale Rao, 1933 and Schistosoma spindale three Schistosoma species are parasites of Artiodactyla, in (Montgomery, 1906), as well as other trematodes such as particular of buffaloes, cows, goats pigs and sheep. Two Echinostoma spp. and some spirorchids (Digenea: of the species cause intestinal schistosomiasis, whilst S. Spirorchiidae)[1,2]. A third species of Schistosoma, Schis- nasale inhabits blood vessels of the nasal mucosa and tosoma indicum (Montgomery, 1906) is also transmitted causes "snoring disease" in cattle[4]. Surveillance for cat- tle schistosomiasis is generally inadequate and the litera- * Correspondence: [email protected] ture is limited, but some idea of the problem can be 1 State Key Laboratory of Biotherapy, West China Hospital, West China Medical School, Sichuan University, Chengdu 610041, China gained from past small scale studies. Surveys in Sri Lanka Full list of author information is available at the end of the article revealed a prevalence of S. spindale of 31.2% (of 901 cat- © 2010 Liu et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons At- tribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Liu et al. Parasites & Vectors 2010, 3:57 Page 2 of 18 http://www.parasitesandvectors.com/content/3/1/57 tle)[5], whilst in Bangladesh a similarly high prevalence of per year; however, in Plio-Pleistocene humid periods this 36% has been reported[6]. More recently, in Kerala South has risen to 630 mm or more[22]. It has been recognized India, prevalences have been reported of up to 57.3% in that it is the length and severity of the dry season that cattle, 50% in buffalo and 4.7% in goats[3]. influences vegetation type (savanna, rain forest, monsoon In addition to causing disease in cattle, I. exustus has forest, etc) rather than the annual rainfall[23]. The rain- been implicated in outbeaks of cercarial dermatitis in fall in the dry season of Assam is approximately 250 mm, human populations in India[7,8], Laos[9], Malaysia[10] whereas that in Northeast Thailand is only 30-40 and Thailand[11,12]. Cercarial dermatitis results from mm[21]. These observations suggest that the Assam/Ban- the cutaneous allergic reaction in people exposed to lar- gladesh populations are subject to different ecological val schistosomes (cercariae) shed by infected snails into conditions than those of the Southeast Asian mainland freshwater bodies such as lakes, ponds, and paddy fields. (SEAM); these observations support the need to question The cercariae cause pruritis and papular eruptions, with the monophyly of Indoplanorbis. The invasive nature and often severe secondary infections, as they attempt to ecological tolerance of the snails adds to their importance infect a non-permissive definitive host and die in the in veterinary and medical science. skin[13]. Indoplanorbis exustus (see Additional file 1) is a com- The historical biogeography of Indoplanorbis mon snail across Southeast Asia and the Indian sub-con- The Lymnaeae and Planorbidae appear to share a com- tinent, where it often acts as intermediate host for S. mon ancestor in the Permian (c.a. 250 Ma (Mega annum spindale. The snail is also found in the Middle East or million years ago)) fossil record[24]. Fossil Planorbinae (Oman and Socotra) and Nigeria and the Ivory Coast; and Bulininae are known from the mid to upper Creta- these findings were attributed by Brandt[14] to recent ceous of Africa and India[25]. The Tethys sea separated introductions by human activities (Brandt's view has Africa and Laurasia until 10-5 Ma[26]. Consequently, been frequently cited in the literature on Indoplanor- Meier-Brook 1984[27] adopted an African (Gondwanan) bis[15-17]). In view of the wide geographical range of this origin for Indoplanorbis with rafting to Asia since the snail and its importance as a host for several species of Cretaceous on the northward migrating Indian craton; Schistosoma, there is a need to understand the phyloge- this author also considered a Europe to Southwest Asia netics and dispersal history of Indoplanorbis. In contrast tract or an Africa to South India dispersal. Morgan et al. to Asia, the well documented appearance of the snail in 2002 attributed the occurrence of Indoplanorbis in India Africa (e.g., Nigeria[18] and Ivory Coast[19]) and more to colonization (from Africa) via the Middle East land recently (2002) in the Lesser Antilles[16], is almost cer- connection[28]. Similarly, Attwood et al. 2007 described a tainly the result of introductions through human activi- Sinai-Levant dispersal tract, from Africa to central Asia, ties over the last 50-100 years. for Schistosoma spindale during the early Pleistocene[29]. Indoplanorbis exustus is a hermaphroditic invasive Clearly the two different dispersal mechanisms imply snail species with high fecundity. Within one year of very different chronologies; the Gondwanan vicariance introduction the snail is able to colonize habitats with hypothesis implies that proto-Indoplanorbis has been well established populations of other pulmonate and present in India since the late Eocene (35 Ma; India: Asia prosobranch snails[16]. The snail requires a water tem- collision[30]), whereas dispersal via the Sinai-Levant sug- perature in excess of 15°C for maturation. At the opti- gests a Plio-Pleistocene arrival. mum temperature of 30°C each snail can lay up to 800 The assumption that the Indoplanorbis lineage has eggs[20]. The capacity for self-fertilization and high been represented on the Indian craton since the Creta- fecundity probably underlies the invasive potential of the ceous is difficult justify in palaeogeographic terms. There species. The snail is found in small ponds, pools and less would have been numerous opportunities for dispersal of commonly in rice paddy fields. The snail may also occur Gondwanan taxa off India and into Asia throughout the in semi-permanent pools formed in flooded areas of Cenozoic. For example, during the middle Eocene (45 fields, where it can survive the dry season buried in mud. Ma) the northern corner of greater India came into con- Consequently, dispersal may occur in clumps of mud tact with western Indonesia and subsequently with adhered to the bodies of cattle or across water in flotsam Sumatra and Myanmar[30]. Even prior to the true (hard) (vegetation mats), and possibly also attached to migratory collison of India with Asia (i.e., between the Indian craton birds (although this has not been observed for I. exustus). and the Lhasa block at 35 Ma), faunal exchange was pos- In Northeast Thailand, where I. exustus is very common, sible via volcanic arc terranes (some forming exposed pla- the annual rainfall is 1541 mm. In Assam, in the region teaus) in the oceanic crust subducting at the collision where the snails were sampled for this study, the annual zone (c.a.